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Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice.

Gallardo CM, Darvas M, Oviatt M, Chang CH, Michalik M, Huddy TF, Meyer EE, Shuster SA, Aguayo A, Hill EM, Kiani K, Ikpeazu J, Martinez JS, Purpura M, Smit AN, Patton DF, Mistlberger RE, Palmiter RD, Steele AD - Elife (2014)

Bottom Line: Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive.To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA.These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, United States.

ABSTRACT
Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive. In this study, we show that mice lacking the dopamine D1 receptor (D1R KO mice) manifest greatly reduced FAA, whereas mice lacking the dopamine D2 receptor have normal FAA. To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA. Within the dorsal striatum, the daily rhythm of clock gene period2 expression was markedly suppressed in D1R KO mice. Pharmacological activation of D1R at the same time daily was sufficient to establish anticipatory activity in wild-type mice. These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

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Individual mouse normalized high activity data from n = 6, D1R KO mice on day 0 and day 21 of 60% CR diet.DOI:http://dx.doi.org/10.7554/eLife.03781.007
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fig2s3: Individual mouse normalized high activity data from n = 6, D1R KO mice on day 0 and day 21 of 60% CR diet.DOI:http://dx.doi.org/10.7554/eLife.03781.007

Mentions: We have added an additional supplemental figure to show 6 individual mice on day 0, the first day of scheduled feeding, and 6 individual mice day 21. We chose day 0 because day -7 is what we consider the “habituation” day as it is the first time the mice have been transported to the video recording room and placed in front of the cameras. In Figure 2–figure supplement 2, randomly selected wild-type mice are shown and in Figure 2–figure supplement 3, 6 randomly selected D1R KO mice are shown. While it is difficult to quantitatively define FAA (in the past we have used the ratio of night time activity peak to FAA peak greater than 0.5), it appears that 2 out of 6 D1R KO mice show some FAA whereas all WT mice show strong FAA on day 21. We do not intend to argue that D1R KO mice have no FAA just that it is attenuated and sometimes absent.


Dopamine receptor 1 neurons in the dorsal striatum regulate food anticipatory circadian activity rhythms in mice.

Gallardo CM, Darvas M, Oviatt M, Chang CH, Michalik M, Huddy TF, Meyer EE, Shuster SA, Aguayo A, Hill EM, Kiani K, Ikpeazu J, Martinez JS, Purpura M, Smit AN, Patton DF, Mistlberger RE, Palmiter RD, Steele AD - Elife (2014)

Individual mouse normalized high activity data from n = 6, D1R KO mice on day 0 and day 21 of 60% CR diet.DOI:http://dx.doi.org/10.7554/eLife.03781.007
© Copyright Policy - open-access
Related In: Results  -  Collection

License
Show All Figures
getmorefigures.php?uid=PMC4196120&req=5

fig2s3: Individual mouse normalized high activity data from n = 6, D1R KO mice on day 0 and day 21 of 60% CR diet.DOI:http://dx.doi.org/10.7554/eLife.03781.007
Mentions: We have added an additional supplemental figure to show 6 individual mice on day 0, the first day of scheduled feeding, and 6 individual mice day 21. We chose day 0 because day -7 is what we consider the “habituation” day as it is the first time the mice have been transported to the video recording room and placed in front of the cameras. In Figure 2–figure supplement 2, randomly selected wild-type mice are shown and in Figure 2–figure supplement 3, 6 randomly selected D1R KO mice are shown. While it is difficult to quantitatively define FAA (in the past we have used the ratio of night time activity peak to FAA peak greater than 0.5), it appears that 2 out of 6 D1R KO mice show some FAA whereas all WT mice show strong FAA on day 21. We do not intend to argue that D1R KO mice have no FAA just that it is attenuated and sometimes absent.

Bottom Line: Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive.To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA.These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

View Article: PubMed Central - PubMed

Affiliation: Division of Biology, California Institute of Technology, Pasadena, United States.

ABSTRACT
Daily rhythms of food anticipatory activity (FAA) are regulated independently of the suprachiasmatic nucleus, which mediates entrainment of rhythms to light, but the neural circuits that establish FAA remain elusive. In this study, we show that mice lacking the dopamine D1 receptor (D1R KO mice) manifest greatly reduced FAA, whereas mice lacking the dopamine D2 receptor have normal FAA. To determine where dopamine exerts its effect, we limited expression of dopamine signaling to the dorsal striatum of dopamine-deficient mice; these mice developed FAA. Within the dorsal striatum, the daily rhythm of clock gene period2 expression was markedly suppressed in D1R KO mice. Pharmacological activation of D1R at the same time daily was sufficient to establish anticipatory activity in wild-type mice. These results demonstrate that dopamine signaling to D1R-expressing neurons in the dorsal striatum plays an important role in manifestation of FAA, possibly by synchronizing circadian oscillators that modulate motivational processes and behavioral output.

Show MeSH